Mini reviewCellulose digestion in termites and cockroaches: What role do symbionts play

What helps termites digest wood

Comparative Biochemistry and Physiology Part B: Comparative Biochemistry

1. Termites and cockroaches are excellent models for studying the role of symbionts in cellulose digestion in insects: they eat cellulose in a variety of forms and may or may not have symbionts.

2. The wood-eating cockroach, Panesthia cribrata, can be maintained indefinitely, free of microorganisms, on a diet of crystalline cellulose. Under these conditions the RQ is 1, indicating that the cockroach is surviving on glucose produced by endogenous cellulase.

3. The in vitro rate at which glucose is produced from crystalline cellulose by gut extracts from P. cribrata and Nasutitermes walkeri is comparable to the in vivo production of CO2 in these insects, clearly indicating that the rate of glucose production from crystalline cellulose is sufficient for their needs.

4. In all termites and cockroaches examined, cellulase activity was found in the salivary glands and predominantly in the foregut and midgut. These regions are the normal sites of secretion of digestive enzymes and are either devoid of microorganisms (salivary glands) or have very low numbers.

5. Endogeneous cellulases from termites and cockroaches consist of multiple endo-ฮฒ-1,4-glucanase (EC 3.2.1.4) and ฮฒ-1,4-glucosidase (EC 3.2.1.21) components. There is no evidence that an exo-ฮฒ-1,4-glucanase (cellobiohydrolase) (EC 3.2.1.91) is involved in, or needed for, the production of glucose from crystalline cellulose in termites or cockroaches as the endo-ฮฒ-1,4-glucanase components are active against both crystalline cellulose and carboxymethylcellulose.

6. There is no evidence that bacteria are involved in cellulose digestion in termites and cockroaches. The cellulase associated with the fungus garden of M. michaelseni is distinct from that in the midgut; there is little indication that the fungal enzymes are acquired or needed. Lower termites such as Coptotermes lacteus have Protozoa in their hindgut which produce a cellulase(s) quite distinct from that in the foregut and midgut.

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How does the Dinobryon eat, and what helps termites digest wood?

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Dinobryon are a type of Chrysophyceae or golden brown algae that reside in freshwater–specifically temperate lakes. They have two methods of obtaining nutrients. They can ingest bacteria by phagotrophy. They are in turn eaten by copepods and Daphnia (water fleas). By ingesting bacteria, they are able to incorporate the carbon from these bacteria into the food chain of the lake. They can also carry out phototrophyand can use light energy to obtain carbon.

Dinobryon are a type of Chrysophyceae or golden brown algae that reside in freshwater–specifically temperate lakes. They have two methods of obtaining nutrients. They can ingest bacteria by phagotrophy. They are in turn eaten by copepods and Daphnia (water fleas). By ingesting bacteria, they are able to incorporate the carbon from these bacteria into the food chain of the lake. They can also carry out phototrophy and can use light energy to obtain carbon in the production of sugar. They fill an important role as both consumer and producer in freshwater lakes and are known as a mixotroph.

Termites are consumers of wood. Because wood contains mainly ligno-cellulose fibers, the digestion of this material requires the presence of specific hydrolytic enzymes. Wood cellulose is a polysaccharide–a carbohydrate consisting of long chains of sugar molecules.

Termites can secrete some cellulose enzymes (cellulases) but they also rely on enzymes from the symbiotic microorganisms residing in their gut to assist with the digestion of their food. One method of breaking down the carbohydrates is fermentation by some of the gut microbes. Others produce methane gas as a by-product of the digestion of wood.

There are many different populations of microorganisms that are responsible for the digestion of lignin and cellulose–some are anaerobic and some aerobic. Different environmental conditions are present in the hind and mid-gut and the residents are separated according to whether they are aerobic or anaerobic. The symbionts living in the termite gut include different types of bacteria, archaea and protozoa.

I have included a link with excellent pictures of the residents inside a termite’s digestive tract.

www.enotes.com

Understanding termite digestion could help biofuels, insect control

February 18, 2013 ะ’

WEST LAFAYETTE, Ind. โ€“ A termite’s own biology with help from microorganisms called protists, are keys to the insect’s digestion of woody material, according to a Purdue University scientist.

Michael Scharf, the O. Wayne Rollins/Orkin Endowed Chair in Urban Entomology, studies termite digestion to improve biofuels production and find better ways to control termites. The U.S. Department of Agriculture estimates the cost of controlling termites and repairing damaged homes is $2 billion each year in the United States.

Much of the study on how termites break down woody materials, which focused on the symbiotic relationship between the insect and the bacteria living in its gut, found that bacteria apparently have little, if anything, to do with termite digestion.

Scharf and collaborators at the University of Florida wanted to see how diet affected those bacteria. If the bacteria play a role in digestion, the type of materials the insect eats should affect the composition of the bacterial community living in the termite gut.

More than 4,500 different species of bacteria were cataloged in termite guts. When multiple colonies of termites were independently fed diets of wood or paper, however, those bacteria were unaffected.

“You would think diet would cause huge ecological shifts in bacterial communities, but it didn’t. We didn’t detect any statistical differences,” Scharf said.

What they did see were far more significant changes in gene expression in the termites and the protists that live in the insects’ guts along with the bacteria.

“The bacteria communities seem very stable, but the host and the protozoa gene expression are changing a lot based on diet,” Scharf said.

The scientists looked at 10,000 gene sequences from the termites and protists to determine which genes were expressed based on differing diets. Termites and protists fed woody and lignin-rich diets changed expression of about 500 genes, leading Scharf to believe those genes might be important for breaking down lignin, a rigid material in plant cell walls that isn’t easily broken down when making biofuels.

“We see much more of the playing field now,” Scharf said.

Understanding which genes are involved in digestion should help researchers track down the enzymes that actually break down woody materials in termite digestion. Those enzymes may be tools scientists could use to better break down biomass and extract sugars during biofuel production.

The National Science Foundation, the Consortium for Plant Biotechnology Inc. and the U.S. Department of Energy funded the research.

The findings were detailed in three papers published in the journals Molecular Ecology, Insect Molecular Biology, and Insect Biochemistry and Molecular Biology.

Writer: Brian Wallheimer, 765-496-2050, [email protected]

Source: Michael Scharf, 765-496-6710, [email protected]

ABSTRACT

The Hindgut Lumen Prokaryotic Microbiota of the Termite Reticulitermes Flavipes and its Responses to Dietary Lignocellulose Composition

Drion G. Boucias, Yunpeng Cai, Yijun Sun, Verena-Ulrike Lietze, Ruchira Sen, Rhitoban Raychoudhury, Michael E. Scharf

Reticulitermes flavipes (Isoptera: Rhinotermitidae) is a highly eusocial insect that thrives on recalcitrant lignocellulosic diets through nutritional symbioses with gut-dwelling prokaryotes and eukaryotes. In the R. flavipes hindgut, there are up to 12 eukaryotic protozoan symbionts; the number of prokaryotic symbionts has been estimated in the hundreds. Despite its biological relevance, this diverse community, to date, has been investigated only by culture- and cloning-dependent methods. Moreover, it is unclear how termite gut microbiomes respond to diet changes and what roles they play in lignocellulose digestion. This study utilized high-throughput 454 pyrosequencing of 16S V5-V6 amplicons to sample the hindgut lumen prokaryotic microbiota of R. flavipes and to examine compositional changes in response to lignin-rich and lignin-poor cellulose diets after a 7-day feeding period. Of the

475,000 high-quality reads that were obtained, 99.9% were annotated as bacteria and 0.11% as archaea. Major bacterial phyla included Spirochaetes (24.9%), Elusimicrobia (19.8%), Firmicutes (17.8%), Bacteroidetes (14.1%), Proteobacteria (11.4%), Fibrobacteres (5.8%), Verrucomicrobia (2.0%), Actinobacteria (1.4%) and Tenericutes (1.3%). The R. flavipes hindgut lumen prokaryotic microbiota was found to contain over 4,761 species-level phylotypes. However, diet-dependent shifts were not statistically significant or uniform across colonies, suggesting significant environmental and/or host genetic impacts on colony-level microbiome composition. These results provide insights into termite gut microbiome diversity and suggest that (i) the prokaryotic gut microbiota is much more complex than previously estimated, and (ii) environment, founding reproductive pair effects and/or host genetics influence microbiome composition.

ABSTRACT

Comparative Metatranscriptomic Signatures of Wood and Paper Feeding in the Gut of the Termite Reticulitermes flavipes (Isoptera: Rhinotermitidae)

R. Raychoudhury, R. Sen, Y. Cai, Y. Sun, V-U Lietze, D. G. Boucias, M.E. Scharf

Termites are highly eusocial insects that thrive on recalcitrant materials like wood and soil and thus play important roles in global carbon recycling and also in damaging wooden structures. Termites, such as Reticulitermes flavipes (Rhinotermitidae), owe their success to their ability to extract nutrients from lignocellulose (a major component of wood) with the help of gut-dwelling symbionts. With the aim to gain new insights into this enzymatic process we provided R. flavipes with a complex lignocellulose (wood) or pure cellulose (paper) diet and followed the resulting differential gene expression on a custom oligonucleotide-microarray platform. We identified a set of expressed sequence tags (ESTs) with differential abundance between the two diet treatments and demonstrated the source (host/symbiont) of these genes, providing novel information on termite nutritional symbiosis. Our results reveal: (1) the majority of responsive wood- and paper-abundant ESTs are from host and symbionts, respectively; (2) distinct pathways are associated with lignocellulose and cellulose feeding in both host and symbionts; and (3) sets of diet-responsive ESTs encode putative digestive and wood-related detoxification enzymes. Thus, this study illuminates the dynamics of termite nutritional symbiosis and reveals a pool of genes as potential targets for termite control and functional studies of termite-symbiont interactions.

ABSTRACT

Lignin-Associated Metagene Expression in a Lignocellulose-Digesting Termite

Amit Sethi, Jeffrey M. Slack, Elena S. Kovaleva, George W. Buchman, Michael E. Scharf

Lignin is a component of plant biomass that presents a significant obstacle to biofuel production. It is composed of a highly stable phenylpropanoid matrix that, upon degradation, releases toxic metabolites. Termites have specialized digestive systems that overcome the lignin barrier in wood lignocellulose to efficiently release fermentable simple sugars; however, how termites specifically degrade lignin and tolerate its toxic byproducts remains unknown. Here, using the termite Reticulitermes flavipes and its symbiotic (protozoan) gut fauna as a model system, we used high throughput Roche 454-titanium pyrosequencing and proteomics approaches to (i) experimentally compare the effects of diets containing varying degrees of lignin complexity on host-symbiont digestome composition, (ii) deeply sample host and symbiont lignocellulase diversity, and (iii) identify promising lignocellulase candidates for functional characterization. In addition to revealing over 9,500 differentially expressed transcripts related to a wide range of physiological processes, our findings reveal two detoxification enzyme families not generally considered in connection with lignocellulose digestion: aldo-keto reductases and catalases. Recombinant versions of two host enzymes from these enzyme families, which apparently play no roles in cellulose or hemicellulose digestion, significantly enhance lignocellulose saccharification by cocktails of host and symbiont cellulases. These hypothesis-driven results provide important new insights into (i) dietary lignin as a xenobiotic challenge, (ii) the complex mechanisms used by termites to cope with their lignin-rich diets, and (iii) novel lignin-targeted enzymatic approaches to enhance biofuel and biomaterial production.

www.purdue.edu

Lower Termite Associations with Microbes: Synergy, Protection, and Interplay

Lower-termites are one of the best studied symbiotic systems in insects. Their ability to feed on a nitrogen-poor, wood-based diet with help from symbiotic microbes has been under investigation for almost a century. A unique microbial consortium living in the guts of lower termites is essential for wood-feeding. Host and symbiont cellulolytic enzymes synergize each other in the termite gut to increase digestive efficiency. Because of their critical role in digestion, gut microbiota are driving forces in all aspects of termite biology. Social living also comes with risks for termites. The combination of group living and a microbe-rich habitat makes termites potentially vulnerable to pathogenic infections. However, the use of entomopathogens for termite control has been largely unsuccessful. One mechanism for this failure may be symbiotic collaboration; i.e., one of the very reasons termites have thrived in the first place. Symbiont contributions are thought to neutralize fungal spores as they pass through the termite gut. Also, when the symbiont community is disrupted pathogen susceptibility increases. These recent discoveries have shed light on novel interactions for symbiotic microbes both within the termite host and with pathogenic invaders. Lower termite biology is therefore tightly linked to symbiotic associations and their resulting physiological collaborations.

Introduction

The close association of lower termites with microbes is fundamental to their biology. For the last century, understanding the intricacies of the relationship between termites and their gut symbionts, i.e., the termite holobiont, has been a major focus of termite research. The majority of this work emphasizes both the complexity and novelty of functions carried out to process lignocellulose within the termite gut (reviewed in Brune, 2014). For decades, termite wood digestion has been a quintessential example of symbiotic collaboration; however, symbionts have also been associated with a myriad of other functions in this system (reviewed in Ohkuma, 2008). For example, in addition to synergistic digestive collaboration, symbionts of lower termites have also been shown to play protective roles against pathogens both in vivo and ex vivo (Rosengaus et al., 1998, 2014; Chouvenc et al., 2009, 2013). This interaction between the termite symbiotic consortium and potential pathogens adds a layer of interplay within this already-complex microbial community. Here we summarize the diversity and roles symbionts play in lower termites, highlight the broad implications of both topics for understanding termite biology and symbiotic evolution, and emphasize how a holistic approach to studying termite biology is necessary to encompass the impact of this obligate symbiotic association.

Lower termites are distinct from higher-termites in that they form relationships with both eukaryotic and prokaryotic symbionts within their digestive tracts (Eutick et al., 1978). While the diversity, abundance, and functionality of these symbionts fluctuates from species to species, an association with symbionts is ubiquitous and connected with much of the biology of termites. Fundamental defining aspects of lower termites, from eusociality to niche occupation, are impacted by their obligate association with microbes. Disruption of this community impacts termite physiological function, fitness, and survivorship (Cleveland, 1924; Thorne, 1997; Rosengaus et al., 2011b, 2014; Peterson et al., 2015; Sen et al., 2015). Lower termites house protists (unicellular eukaryotes), bacteria, and archaea all within the one-microliter environment of their hindgut, many of which are never found outside of this association. Restricted to their association with termites, these symbionts are exposed to and must tolerate a variety of chemical and biological stressors in the termite gut microenvironment. As the host termite feeds, forages, grows, and encounter pathogens, its symbiota are impacted. Thus, termites cannot be studied without also considering their symbionts. Characterizing and cataloging these microbes poses many challenges because most are unable to be cultured with traditional techniques due to their fastidious nature. This gut microenvironment boasts organismal and metabolic diversity which rivals some of the better studied macro-ecosystems. Approaching the termite holobiont as a fully functional, multifaceted ecosystem allows for concentration on individual species or processes and on the larger collaborative nature of the gut microenvironment.

Characterizing the Lower Termite Gut Consortium

The key division between lower and higher termite species is the respective nature of their symbiotic partners. While both retain prokaryotic symbionts, lower termites also have flagellated protists living in their guts which is an ancestral trait shared with wood-feeding cockroaches, Cryptocercus sp. (Stingl and Brune, 2003; Lo and Eggleton, 2011; Brune and Dietrich, 2015). These protists belong to two groups: the oxymonads and the parabasalids. Originally described as parasites, protists were first found associated with termites over a century ago (Leidy, 1877). Since this original observation, roughly 500 termite-associated protist species have been described (reviewed in Ohkuma and Brune, 2011). As technology advances we are continually able to improve our understanding of the players and complexity of the termite gut community. In fact, new species of protistan symbionts are continually described from lower termite guts (Brugerolle and Bordereau, 2004; Gile et al., 2012; James et al., 2013; Tai et al., 2013; Radek et al., 2014), and the breadth of their diversity is thought to be drastically underestimated in general (Harper et al., 2009; Tai and Keeling, 2013). That being said, lower termites are thought to possess anywhere from a few to a dozen protist species as symbionts that maintain tight phylogenetic associations with their hosts (Tai et al., 2015).

As has happened with protist symbionts, our understanding of the bacterial consortium composition in lower termites is constantly evolving as methodologies and analyses improve. Early estimates from the eastern subterranean termite, Reticulitermes flavipes, numbered bacteria per gut in the millions, which seems to be a conservative approximation at best (Schultz and Breznak, 1978). Using culture-independent, cloning based methods, several groups have estimated the guts of lower termite species to contain anywhere from 222โ€“1,318 ribotypes of bacteria (Hongoh et al., 2003a,b; Shinzato et al., 2005; Yang et al., 2005; Fisher et al., 2007). With the onset of next-generation sequence technologies this number has only grown. More recently, the gut lumen content of R. flavipes workers was described to contain over 4,761 species-level phylotypes of prokaryotic symbionts, with over 99% being bacteria (Boucias et al., 2013). The majority of these identified phylotypes are unique to the termite gut, having never been reported elsewhere and not having close-relative sequences available in databases. Coptotermes gestroi has been estimated to house 1,460 species of bacteria using Illumina technology (Do et al., 2014). These estimates vary for a variety of possible reasons, including local environment, study locus, methodological limitations/caveats, sampling strategy, diet, genetic background, and termite species. While identifying the microbial players within this system is an important step, describing the functions and interplay between them will be equally necessary for understanding termite biology and evolution.

Symbiotic Collaboration in Termite Digestion and Nutrition

Apart from cataloging symbiont diversity, much of termite research has focused on their associations with the symbiotic microbes which aid in wood digestion. Feeding on this lignin-rich, nitrogen-poor diet requires a suite of enzymes both to catalyze its breakdown and supplement its nutritional deficiencies. Termites and their symbionts complement each otherโ€™s capabilities in this way. Termites contribute several highly active enzymes important to this process including endogenous cellulases (ฮฒ-1, 4-endoglucanase, ฮฒ-glucosidase) and lignin/phenolic detoxifiers (aldo-keto reductase, laccase, catalase, cytochrome p450s) (Scharf et al., 2010; Zhou et al., 2010; Raychoudhury et al., 2013; Sethi et al., 2013b). Protists in the hindgut of lower termites have been credited with the contribution of several important glycosyl hydrolases (GHFs 5, 7, 45) which aid in cellulolytic activity (Ohtoko et al., 2000; Todaka et al., 2010; Sethi et al., 2013a) and are important in hydrogen cycling (Inoue et al., 2005, 2007). Based on transcriptomic studies, protists possess many more potentially important cellulases (Todaka et al., 2007; Tartar et al., 2009). Also, both the termite host and protist symbionts possess proteases which may be important for utilizing bacteria as sources of nitrogenous compounds (Sethi et al., 2011; Tokuda et al., 2014). Although both protists and bacteria possess many hemicellulases (Inoue et al., 1997; Tartar et al., 2009; Tsukagoshi et al., 2014), termite endogenous cellulases have been shown to have hemicellulase activity as well (Scharf et al., 2010, 2011; Karl and Scharf, 2015). However, despite this apparent hemicellulolytic redundancy, protists, bacteria, and archaea in the hindgut paunch clearly all contribute significantly to the overall efficiency of wood digestion (Peterson et al., 2015).

While protists are mainly responsible for lignocellulolytic activity, the prokaryotic community provides a more diverse subset of services in the termite gut. Spirochetes, the most conspicuous bacterial group in lower termite guts, are capable of diverse metabolic processes including acetogenesis, nitrogen fixation, and degradation of lignin phenolics (Lilburn et al., 2001; Graber and Breznak, 2004; Lucey and Leadbetter, 2014). The isolation and maintenance of pure cultures of several species of spirochetes from lower termite guts has been a powerful tool for describing their metabolic capabilities and collaborative potential within the community as a whole (Leadbetter et al., 1999; Lilburn et al., 2001; Salmassi and Leadbetter, 2003; Graber and Breznak, 2004, 2005; Graber et al., 2004; Drรถge et al., 2006; Rosenthal et al., 2011).

Another major component of lower termite microbiota are the bacteria which are intimately associated with gut flagellates as intracellular endosymbionts (Stingl et al., 2005; Noda et al., 2009). There are four phyla of bacterial endosymbionts found within protist cells: Elusimicrobia, Bacteroidetes, Proteobacteria, and Actinobacteria (Hara et al., 2004; Noda et al., 2005; Stingl et al., 2005; Strassert et al., 2012). These groups have been found to ferment glucose, synthesize amino acids, produce cofactors, fix nitrogen, and recycle nitrogenous wastes (Noda et al., 2007; Hongoh et al., 2008a,b; Ohkuma and Brune, 2011; Strassert et al., 2012; Zheng et al., 2015). Methanobrevibacter, a methanogenic archaeal genus common across termite-associated flagellates, contribute methane to the gut environment using hydrogen that is present in copious amounts in the gut lumen as a product of cellulose metabolism (Shinzato et al., 1999; Tokura et al., 2000; Hara et al., 2004; Hongoh and Ohkuma, 2011). This adds another level of complexity to termite gut ecology by creating a tripartite symbiosis: prokaryotes within protozoa within termites.

Apart from archaea associated with termite gut flagellates, representative Methanobacteriaceae are also associated with the microaerobic termite gut lining (Leadbetter and Breznak, 1996; Ohkuma et al., 1999; Brune, 2011). Together with the flagellate endosymbiota, the large amount of methane created by termite digestion can be attributed to archaea which are typically associated with the hindgut lining (Brune, 2011; Hongoh and Ohkuma, 2011). In sum, the microbes present in lower termite guts comprise a diverse ecosystem capable of nitrogen cycling, carbohydrate metabolism, methanogenesis, amino acid biosynthesis, hydrogen turnover, and consequently, complementing deficiencies of the host.

In addition to the contributions of individual organisms, the host fraction (foregut, midgut, and salivary glands) and the symbiont fraction (hindgut) of the termite digestive system have been shown to work synergistically (Scharf et al., 2011). While both fractions have lignocellulolytic activity, combining protein extracts from both the host and symbiont fractions results in more sugar release in vitro than the sum of the parts. Additionally, recombinant host and symbiont enzymes have been shown to work efficiently in vitro to liberate glucose and pentose sugars from wood (Sethi et al., 2013a). Hence, wood digestion is truly the result of successful collaboration between termites and their hindgut symbionts. This collaborative physiological functionality is a driver in termite success and niche occupation, and it should continue to be a major focus to understand termite holobiont biology and ecology as we go forward.

Symbiontโ€“Pathogen Interplay

Social living and foraging in microbe-rich environments puts termite workers at risk to encounter pathogens and creates the potential for epizootic events within termite colonies. Though the relationship between termites and their symbionts is often perceived to be purely nutritional, there is growing evidence that gut microbiota have infection-buffering potential. However, termites also have evolved complex hygienic behaviors to mitigate the spread and persistence of pathogenic agents (i.e., fungal conidia) within colonies (Rosengaus et al., 1998; Rosengaus et al., 2011a; Gao et al., 2012). Termites have been frequently observed to auto- and allogroom conidia from the bodies of themselves and nestmates. Passage through the alimentary canal and symbiont-filled hindgut effectively neutralizes fungal conidia (Chouvenc et al., 2009). Termites with perturbed gut microbiota, by oxygenation or chemical means, display a marked increase in susceptibility to fungal pathogens such as Metarhizium anisopliae and Beauveria bassiana (Boucias et al., 1996; Ramakrishnan et al., 1999; Rosengaus et al., 2014; Sen et al., 2015). One biochemical mechanism has been linked to this anti-fungal gut phenomenon in the form of symbiont-derived ฮฒ-1, 3-glucanase activity (most likely protist) that is able to act on fungi and prevent their germination (Rosengaus et al., 2014). Similarly, the inhibition of this antifungal enzyme activity, ฮฒ-1, 3-glucanase, results in a marked increase in termite susceptibility to a variety of pathogens (Bulmer et al., 2009) and is conserved evolutionarily from woodroaches to termites (Bulmer et al., 2012).

As mentioned above, grooming and hygienic behavior play an important role in termite immunity. Termites also participate in proctodeal trophallaxis as a means to replenish symbionts, nutrients, and chemical signals amongst individuals in the colony (Suarez and Thorne, 2000; Machida et al., 2001). This is another means by which symbionts and potential pathogens may interact, but it does not seem to play an important role in immune priming (Mirabito and Rosengaus, 2016).

Lastly, outside of the termite body, symbiotic bacteria provide additional protection. Termites build elaborate nest structures from fecal material to house their colonies. As with hindgut populations, these nest materials contain varying degrees of microbial abundance and richness dependent upon the species of termite (Rosengaus et al., 2003). This material contains diverse kinds of bacteria but has comparatively less fungus (Rosengaus et al., 2003; Manjula et al., 2015). The nests of one species of subterranean termite, Coptotermes formosanus, are commonly laden with symbiotic Actinobacteria demonstrated to have antifungal activity ex vivo in nest walls (Chouvenc et al., 2013). This finding extends symbiont-mediated protection from the termite gut outside into the nest material, in at least one species.

Concluding Remarks

Lower termite symbioses with microorganisms are unmistakably integral to termite biology. Hindgut microbial communities are tightly linked with termite digestion of wood and play important roles in supplementing this nutrient-poor food source. Symbionts catalyze reactions involved in the breakdown of all three major components of wood (cellulose, hemicellulose, and lignin phenolics) and supplement this diet by synthesizing other important nutrients. However, outside of the classic role for termite symbionts in digestion and nutrition, there is increasing recognition that they buffer the impacts of environmental stressors to their hosts. In particular, both protists and bacteria have been found to provide anti-fungal defenses in lower termites (Chouvenc et al., 2013; Rosengaus et al., 2014). Even fitness is impacted by the interconnectivity between termites and their symbionts (Rosengaus et al., 2011b). Recent discoveries emphasize that despite nearly a century of studying the obligate relationships between lower termites and microbes, there are still many facets of this complex association which are yet to be understood. Lower termites provide an important model for studying persistent, multi-layer symbioses.

It is also important to consider the role that symbiota play in other animal systems for the purpose of formulating relevant questions to probe, interrogate and eventually understand the termite holobiont. Recent discoveries in other models highlight microbiota as playing more active roles in host physiology, development, and behavior. These roles extend further than the bounds of the intestinal walls, affecting a range of processes from immune system development/maturation to mood and pain perception (Sommer and Backhed, 2013). The broad influence of gut microbiota found in these other systems can serve as an excellent guide to generate hypotheses for testing in the termite system.

Moving forward, based on recent and emerging trends, it will be imperative to consider all components of the termite holobiont when investigating aspects of termite biology. Understanding the role of symbiotic microbes in the physiological processes of digestion and immunity represent some of the first steps toward a better understanding the broader functionality of the lower termite consortium. Viewing any of these interactions within the termite holobiont as discrete may be an oversimplification. However, as methodologies and analyses advance, our ability to understand the functions of the consortium as a whole will continue to improve, as will our understanding of the roles of individual taxa in the system, and collaborations between host and symbiota. Efforts to characterize the holobiont in the presence and absence of stressors, both biotic and abiotic, using comprehensive omics-based approaches are likely to be major hypothesis-generating endeavors. However, the key to doing this successfully will involve careful sample preparation and carefully constructed analysis pipelines to limit taxonomic biases whenever possible. These big data approaches will in turn become a springboard into understanding symbiotic association, trends and commonalities, which may help to begin building models for the compartmentalization, complementation, and collaboration between lower termites and their symbiota.

Understanding the extent, bounds, and ramifications of these associations will be necessary to move toward a fuller appreciation of lower termite biology. Ultimately, studying the collective function and interplay between all members of this symbiosis in response to environmental challenges and in periods of stasis will shed light both on the micro-ecosystem that is a termite gut and the super-organism that is a termite colony.

Author Contributions

BP and MS developed, wrote, and revised the ideas and content presented in this manuscript. Both BP and MS approve the publishing of this manuscript and take responsibility for all of its contents.

Conflict of Interest Statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

The authors acknowledge Dr. S. P. Rajarapu, Dr. M. N. Fardisi, and our reviewers for helpful review, discussion, and comments during revision of this manuscript.

www.ncbi.nlm.nih.gov

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